Christopher N. Balakrishnan

The coevolution of interacting mitochondrial and nuclear genes is increasingly recognized as a critical component of organismal fitness and a potential source of genetic incompatibilities that promote speciation. In species with ‘ZW’ sex chromosomes, however, selection on maternally inherited traits may impact mitonuclear coevolution owing to the effective linkage of the W chromosome and mitochondrial DNA (mtDNA). Here we show that in brood parasitic cuckoo finches (Anomalospiza imberbis), enhanced ecological selection on a maternally inherited trait (mimetic egg colouration) subjects both the W chromosome and mtDNA to increased accumulation of slightly deleterious mutations via genetic hitchhiking, accelerating W chromosome pseudogenization and gene loss, as well as mitonuclear coevolution. Remarkably, as other W-linked genes were lost, two egg colour genes, representing likely targets of selection during cuckoo finch–host coevolution, were recruited to the W chromosome. Using structural models of the respiratory complexes and mitoribosome, we also show that the rate of amino acid substitution in nuclear-encoded residues is a function of their proximity to mtDNA-encoded residues, providing evidence of compensatory mitonuclear coevolution. Our results link species-level coevolution to both sex chromosome degeneration and mitonuclear coevolution. More generally, they highlight the genomic consequences of adaptation without recombination.

Captive breeding can be a key component of species conservation strategies, but also exposes these rare species to novel environments including the pathogen landscape. The critically endangered white‐winged wood duck (WWWD) Asarcornis scutulata has experienced substantial population declines, local extirpations and fragmentation of its former range in Southeast Asia, making it one of the rarest birds in the world. As in other rare species, WWWD declines have led to the initiation of captive breeding programs, but these have been hampered by the WWWDs' high susceptibility to Mycobacterium avium , avian tuberculosis (TB). In this study we describe genome‐wide patterns of diversity to understand the WWWD's demographic and phylogeographic history, inbreeding in the wild and in captivity, and the causes of TB susceptibility. Captive birds, which originated from northeast India, are genetically differentiated from wild birds sampled in Sumatra, Indonesia, likely reflecting long‐standing phylogeographic structure. Demographic analyses revealed that long‐term (Pleistocene) population declines preceded anthropogenic declines, a pattern shared with other codistributed, forest‐dependent species. All sampled WWWD populations had extremely low genetic diversity ( π = 0.0008–0.0015) but wild‐sampled birds retained higher Major Histocompatibility Complex (MHC) diversity, reflecting important functional diversity in the wild. Genetic diversity has eroded over time in captivity and importantly, birds with higher levels of inbreeding succumb earlier to TB infections, suggesting inbreeding depression. Finally, by comparing gene expression between susceptible WWWD and resistant redhead ducks Aythya americana we identify possible mechanisms of TB susceptibility. Altogether our study provides genomically‐guided objectives for future management and a cautionary tale for ex situ conservation.

Parental care evolved as a strategy to enhance offspring survival at the cost of reduced adult survival and fecundity. While 99% of bird species provide parental care, obligate brood parasites circumvent this trade-off by exploiting the parental behaviours of other species. This radical life-history shift occurred independently seven times in birds, offering an outstanding opportunity to test for convergent adaptation. To investigate genomic adaptations underlying this transition, we analyse population resequencing data from five brood-parasitic species across three independent origins of brood parasitism—three parasitic finches, a honeyguide and a cowbird—alongside related non-parasitic outgroups. Using the McDonald–Kreitman framework, we find evidence for adaptation in genes involved in sperm function in multiple parasitic clades, but not in the matched, non-parasitic outgroups, consistent with evidence for increased male–male competition in parasitic lineages following the loss of parental care. We also detect selective sweeps near genes associated with nervous system development in parasitic lineages, perhaps associated with improved spatial cognition that aids brood parasites in locating and monitoring host nests. Finally, we detect more selective sweeps in the genomes of host specialist brood parasites as compared to non-parasitic outgroups, perhaps reflecting ongoing host–parasite coevolutionary arms races.

Odorant receptors (ORs) form one of the largest gene families in vertebrates; most mammals have hundreds of intact OR genes. Although birds display diverse breeding and foraging behaviors, they were long assumed to rely minimally on olfaction. Here we show that, similar to mammals, bird genomes often encode hundreds – and in some species, thousands – of intact ORs. We further present evidence that most avian ORs within the bird-specific gamma-c subfamily have undergone extensive gene conversion. We show that avian ORs are expressed in olfactory sensory neurons and respond to defined odorants. Notably, we identify ligands for avian ORs, revealing both unique functions within the gamma-c clade and functional conservation with a deeply divergent mammalian OR. These findings uncover unexpected parallels between mammals and birds in olfactory system organization while revealing a distinctive evolutionary feature: widespread gene conversion shaping the majority of avian ORs.

Examples of convergent evolution, wherein distantly related organisms evolve similar traits, including behaviors, underscore the adaptive power of natural selection. In birds, obligate brood parasitism, and the associated loss of parental care behaviors, has evolved independently in seven different lineages, though little is known about the genetic basis of the complex suite of traits associated with this rare life history strategy. We generated genome assemblies for ten brood parasitic species plus eight species representatives of their parental/nesting outgroups. This includes nine long-read chromosome-level assemblies, with scaffold N50 sizes ranging from 38.1 to 72.6 MB, and gene representation completeness measures >97%. Leveraging this new catalog of avian genomes, we constructed clade-level alignments that reveal variation in chromosomal synteny, provide first-time or improved annotations of protein-coding and non-coding genes, and define cross-species ortholog reference sets. We also refine estimates for the timing of the seven independent origins of brood parasitism, ranging from recent events such as 1.6–4.5 million years ago in Molothrus cowbirds to much earlier origins over 30 million years ago in two of the three cuckoo lineages. These genomic resources lay the foundation for investigating the genetic and genomic underpinnings of brood parasitism, including the loss of parental care, shifts in mating systems, perhaps resulting in heightened sperm competition, elevated annual fecundity, improved spatial cognition related to nest-finding, and the diverse adaptations shaped by intense coevolution with host species.

The coevolution of interacting mitochondrial and nuclear genes involved in the oxidative phosphorylation (OXPHOS) pathway has received growing attention as a critical component of organismal fitness1 and potential source of genetic incompatibilities2–4 that promote speciation5–7. However, in species with “ZW” sex chromosomes, the mitochondrial genome and female-specific W chromosome are effectively linked by their shared matrilineal history, such that selection on either should subject both to the accumulation of deleterious mutations via genetic hitchhiking8,9. Thus, enhanced ecological selection on maternally inherited traits should accelerate both W chromosome degeneration and mitonuclear coevolution, though this prediction has not been tested empirically. Here we show that brood parasitic cuckoo finches Anomalospiza imberbis, in which mimetic egg coloration is maternally inherited, have experienced accelerated W chromosome pseudogenization and gene loss in addition to higher rates of amino acid substitution in both their mitochondrial and nuclear-encoded OXPHOS genes. Using a structural model of respiratory complex I, we also show that the degree of acceleration in nuclear-encoded residues is a function of their proximity to mtDNA-encoded residues, providing strong evidence of compensatory mitonuclear coevolution. Our results link ecological coevolution at the species level to both sex chromosome degeneration and mitonuclear coevolution, highlighting genomic consequences of selection on non-recombining genome components.

Captive breeding can be a key component of species conservation strategies, but also exposes these rare species to novel environments including the pathogen landscape. The critically endangered white-winged wood duck (WWWD) Asarcornis scutulata has experienced substantial population declines, local extirpations and fragmentation of its former range in South-East Asia, making it one of the rarest birds in the world. Like other rare species, WWWD declines have led to the initiation of captive breeding programs, but these have been hampered by the WWWDs’ high susceptibility to Mycobacterium avium , avian tuberculosis (TB). In this study we describe genome-wide patterns of diversity to understand the WWWD’s demographic and phylogeographic history, inbreeding in the wild and in captivity, and the causes of TB susceptibility. Captive birds, which originated from northeast India, are genetically differentiated from wild birds sampled in Sumatra, Indonesia, likely reflecting long-standing phylogeographic structure. Demographic analyses revealed that long-term (Pleistocene) population declines preceded anthropogenic declines, a pattern shared with other codistributed, forest-dependent species. All sampled WWWD populations had extremely low genetic diversity but wild-sampled birds retained higher Major Histocompatibility Complex (MHC) diversity, reflecting important functional diversity in the wild. Genetic diversity has eroded over time in captivity and importantly, birds with higher levels of inbreeding succumb earlier to TB infections, suggesting inbreeding depression. Finally, by comparing gene expression between susceptible WWWD and resistant redhead ducks Aythya americana we identify possible mechanisms of TB susceptibility in WWWD. Altogether our study provides genomically-guided objectives for future management and a cautionary tale for ex-situ conservation.

Developmental processes emerge from both maturational and experience‐dependent mechanisms. Experience at the proper maturational stage is essential for the acquisition of many complex cognitive and behavioral processes. A striking example of this is a critical period, a restricted developmental phase during which experience is required for both behavioral acquisition and period closure. Juvenile male zebra finches (Taeniopygia castanotis) possess a critical period for song learning; hearing an adult “tutor's” song between posthatch days 30–65 is necessary for each male to produce a socially functional adult song. However, if tutor song is not experienced in this age range, juveniles can still learn beyond posthatch day 65. Our broad objective is to decipher the neurogenomic mechanisms that promote or limit the ability to learn, leveraging the known parameters of the critical period in the male zebra finch's sensory song learning ontogeny. Here, we manipulated juvenile males' tutor exposure and provided song playback experience at two ages, at the beginning or end of the critical period. We probed the relationship between DNA methylation and transcriptional profiles from the same individual and tissue samples to enhance interpretation across different levels of biological organization. Our findings uncovered specific genes and processes that may regulate aspects of critical period learning, as well as aspects of DNA methylation dynamics and how they correspond to RNA measures. Because we distinguished effects of age and experience, outcomes provide insight into fundamental links between epigenetic and molecular properties as the developing brain shifts its ability to learn.

Parental care evolved as a strategy to enhance offspring survival at the cost of reduced fecundity. While most birds provide parental care, obligate brood parasites circumvent this tradeoff by exploiting the parental behavior of other species. This radical life history shift has occurred independently seven times in birds, offering an outstanding opportunity to test for convergent patterns of adaptation in the genome. To investigate genomic adaptations underlying this transition, we analyzed population resequencing data from five brood-parasitic species across three independent origins of brood parasitism — three parasitic finches (family Viduidae), a honeyguide, and a cowbird — alongside related non-parasitic (parental) outgroups. Using the McDonald-Kreitman framework, we found evidence for repeated adaptation in genes involved in spermatogenesis and sperm function in multiple parasitic clades, but not in the matched outgroup parental species. This is consistent with evidence for increased male-male competition in parasitic lineages as a result of the loss of parental care. In addition, we detected selective sweeps near genes associated with nervous system development in parasitic lineages, perhaps associated with improved spatial cognition that aids brood parasites in locating, monitoring, and laying eggs in host nests. Finally, we found more selective sweeps in host-specific brood parasites as compared to parental outgroups, perhaps reflecting ongoing host-parasite coevolutionary arms races.